Herpetology Notes, volume 14: 303-307 (2021) (published online on 09 February 2021)

First records for Europe of the non-native turtles Kinosternon subrubrum Bonnaterre, 1789 and Pelomedusa olivacea (Schweigger, 1812) in a suburban wetland in central Italy

Vincenzo Ferri1,2, Corrado Battisti3,*, Christiana Soccini1, and Riccardo Santoro4

Kinosternon subrubrum Bonnaterre, 1789 is a North colonisation of these ecosystems (Da Silva and Blasco, American semi-aquatic freshwater turtle found primarily 1995; Martinez-Silvestre et al., 2001; Shiau et al., 2006). in the mid-Atlantic and southeastern regions of the United Here, we provided the first records of K. subrubrum and States (Powell et al., 2016). This primarily carnivorous P. olivacea in a suburban wetland remnant in central species prefers lentic freshwater systems, but it also has Italy. These are the first records for Europe, outside the been reported to inhabit brackish marshes (Frazer et respective native geographical ranges of both species. al., 1991; Wilson et al., 1999; Ernst and Lovich, 2009; Study area. The study area is the Palude di Torre Flavia Meshaka et al., 2017). Its longevity in the wild is thought (Battisti, 2006), a 40-ha wetland managed as a protected to exceed 30 yrs (Gibbons, 1983). nature reserve (Special Protection Area IT6030020, Pelomedusa olivacea (Schweigger, 1812) is a according to EU Directives 79/409 and 2009/147/EU) freshwater turtle native to Benin, Burkina Faso, Niger, that is located in the Latium region along the Tyrrhenian Nigeria, and Senegal (Vargas-Ramírez et al., 2010, 2016; coast of central Italy (41.9624°N, 12.0461°E; Fig. 1). Wong et al., 2010; Fritz et al., 2014; Petzold et al., 2014). This ecosystem is the remnant of a larger wetland, It is primarily carnivorous, feeding on amphibians (adults drained and transformed in the second half of the 20th and larvae), fish, crabs, ticks, molluscs, birds, and small Century and embedded in an agricultural and urbanized mammals. The species occupies marshes, temporary landscape (40 km from Rome, 2 km north of Ladispoli pans, pools, or puddles and shows a high vagility, moving – a town with about 40,000 inhabitants). This wetland great distances (Boycott and Bourquin, 2008). is characterized by a seminatural patchiness with ponds Both of these species are included among the freshwater and channels, reedbeds (Phragmites australis), flooded turtles held worldwide as pets, although with less meadows, dunes, and patches of Carex hirta, Juncus frequency compared to large traded species, such as acutus, and Cyperaceae (Guidi, 2006). The area was Trachemys scripta (Ferri and Soccini, 2008; Tapley et managed for fish farming until 2004 (pisciculture of al., 2011; Masin et al., 2014). However, as with many mullet fry, Mugil cephalus, Chelon ramada, and C. other pet species, these turtles are sometimes released by saliens). The water supply comes largely from rainfall their owners into ponds or urban and suburban wetlands (Mesomediterranean Xeric Region; Tomaselli et al., (e.g., Masin et al., 2014), thereby potentially inducing 1973) and from an artificial intake controlled by the park agency managing this reserve (‘Città Metropolitana di Roma Capitale’ Agency). Inflow from surrounding areas is scarce. The area may suffer major hydrological stress, 11 Via Valverde 4, 01016 Tarquinia, Italy. especially in late spring–summer (May–September). 2 Evolutionary Biology and Zoology, Department of Biology, Fires of reedbeds (either controlled or not) are recurrent, University of Rome II ‘Tor Vergata’, Via Cracovia 3, 00133 Rome, Italy. occurring mainly in late summer. 3 ‘Torre Flavia’ Long Term Ecological Research Station, Città Sampling. From 1997, when the Palude di Torre Metropolitana di Roma, Via Tiburtina 691, 00159 Rome, Italy. Flavia was protected as a nature reserve, a large number 4 Via Eugenio Maccagnani 55, 00148 Rome, Italy. of researchers periodically and randomly sampled the * Corresponding author. E-mail: c.battisti@ macrofauna in the water channels (Battisti, 2006). During cittametropolitanaroma.gov.it the months of May–July in the years 2016–18, we carried © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. out a time-constrained systematic sampling survey (SSS; 304 Vincenzo Ferri et al.

Figure 1. Location of Torre Flavia wetland in central Italy, where Kinosternon subrubrum and Pelomedusa olivacea were recorded.

Dodd, 2010) focused on freshwater turtles. Sampling and lakes of Rome, six non-native freshwater turtles were was carried out along three transects (total length: 550 m) recorded, but not these species (Di Santo et al., 2017). randomly located inside the study area. Research effort These records are also the first records of apparently was about 12 h. Specimens were identified following free-ranging individuals for Europe. Records outside Petzold et al. (2014). The collected specimens were their non-native range exist for areas outside of Europe deposited in the zoological collection of Vincenzo Ferri (for Kinosternon subrubrum see Ceballos and Fitzgerald, (Natural Museum of Sant’Oreste, Rome, Italy). 2004; for Pelomedusa sp., see Fujisaki, et al., 2010 and Romagosa, 2014). In the case of P. subrufa, a non-native Results population is known from Spain (Bugter et al., 2011). Pelomedusa olivacea is widely traded in Rome as After the devastating fire of 16 July 2017, we a pet (V. Ferri, pers. obs.). Moreover, in Ladispoli (the recorded a carcass of Kinosternon subrubrum in the town closest to the wetland), there is a large community reedbed (Fig. 2). Species identity was determined of residents with Senegalese origin. It is possible that by examining the remains of the carapace using a turtle, whose range includes the country of origin of characteristics reported by Iverson (1977). These community members, may be held as a pet to memorialize included a first vertebral that does not contact the the homeland and may have escaped or been released. second marginal, a ninth marginal not elevated above It is most likely that either of these turtles are only the preceding marginals, length and width of the occasionally released, and there is no evidence for second vertebral nearly equal, whereas the posterior colonization. The area has high suitability for turtles, vertebrals are wider than long. The straight carapace given the high availability of trophic and spatial resources length was 10.4 cm. (Battisti, 2006). For the Torre Flavia wetland we have During our surveys, we also recorded two carcasses of obtained evidence of a rich community of non-native Pelomedusa olivacea (Fig. 3). At the beginning of April freshwater turtles, represented by at least 10 taxa at the 2017, the carcass of one large adult female was found species and subspecies levels, including Graptemys p. floating at the edge of a pond in an advanced state of pseudogeographica (Gray, 1831), G. p. kohni (Baur, putrefaction. The second specimen was an adult male 1890), Pseudemys c. concinna (Le Conte, 1830), P. nelsoni that had been killed in the fire on 16 July 2017. Carr, 1938, Trachemys scripta elegans (Wied, 1839), T. s. scripta (Schoepff, 1792), T. s. troosti (Holbrook, Discussion 1836), and Mauremys sinensis (Gray, 1834). Therefore, Neither of these two freshwater turtles has previously these two observations corroborate the concern about the been recorded in the Latium region (Bologna et al., 2000, release of pet animals into the wild. 2007; Scalera and Montinaro, 2014) or in Italy (Sindaco et The presence of so many invasive species implies a al., 2006). In a large survey carried out on 31 urban ponds disruption or alteration of ecological relationships, but First European Records for Kinosternon subrubrum and Pelomedusa olivacea 305

Figure 2. (a) Parts of the shell of an Eastern Mud Turtle (Kinosternon subrubrum) of undetermined sex, comprising both skeletal and dermal bone. The specimen was apparently killed by a fire on 16 July 2017. (b) Reconstructed shell. (c) Live specimen of Kinosternon subrubrum. Photos by Vincenzo Ferri (a, b) and courtesy of Austin’s Turtle Page (c). this has yet to be observed in the study area (Amori and non-native species could also compete with the native Battisti, 2008). It would be interesting to carry out studies Emys orbicularis (see Luiselli et al., 1997), which is also on the food web to better understand the role of non- locally present. native freshwater turtles, since this wetland is also home to invasive populations of the crustacean Procambarus Among the freshwater species occurring in this clarkii and the mosquitofish Gambusia holbrooki wetland, some (e.g., Pelomedusa) show a high risk (Chiesa, 2006; Celauro, 2006), which are both potential of potential invasion outside their native range due prey for turtles. Moreover, non-native freshwater turtles to climate matching, coexistence with humans, high may represent a further trophic resource for large fecundity, and human tolerance (Kopecký et al., 2013; predatory birds (e.g., waders, such as herons). However, Masin et al., 2014). In this regard, we suggest improving 306 Vincenzo Ferri et al.

Figure 3. (a–e) Parts of the shell, comprising both skeletal and dermal bone, of two specimens of North-western African Helmeted Turtle, Pelomedusa olivacea, retrieved from Torre Flavia wetland in central Italy. (a, b) Cranium of a large adult female, found floating at the edge of a pond in an advanced state of putrefaction. (c) Lateral view, (d) carapace, and (e) plastron of the remains of an adult male apparently killed by a fire on 16 July 2017. (f) Shown for comparison is a female subadultP . olivacea from the pet market with origin in West Africa. Photos by Vincenzo Ferri and Guido Tavecchio. control of commercial trade, local release, and Editore. 192 pp. eradication projects promoted by the local park agency Boycott, R.C., Bourquin, O. (2008): Pelomedusa subrufa (Lacépède (see Ferri and Soccini, 2008). 1788) – helmeted turtle, helmeted terrapin. In: Conservation Biology of Freshwater Turtles and Tortoises: a Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Acknowledgments. We thank Egidio De Angelis, Carlo Galimberti, Specialist Group. Chelonian Research Monographs 5, p. 007.1–6. and Narciso Trucchia, rangers of Monumento naturale “Palude di Rhodin, A.G.J., Pritchard, P.C.H., Dijk, P.P. van, Saumure, R.A., Torre Flavia”, for their support. Luca Luiselli pre-reviewed a first Buhlmann, K.A., Iverson, J.B., Eds., Lunenburg, Massachusetts, draft of the manuscript. Hinrich Kaiser and an anonymous reviewer USA, Chelonian Research Foundation. provided useful comments and suggestions, which improved the Bugter, R.J.F., Ottburg, F.G.W.A., Roessink, I., Jansman, H.A.H., first draft of the manuscript. We also thank Paolo Crescia for editing Grift, E.A. van der, Griffioen, A.J. (2011): Invasion of the the high-definition images Turtles? Exotic Turtles in the Netherlands: a Risk Assessment. Wageningen, The Netherlands, Alterra report 2186. 92 pp. References Ceballos, C.P., Fitzgerald, L.A. (2004): The trade in native and exotic turtles in Texas. Wildlife Society Bulletin 32: 881–892. Amori, G., Battisti, C. (2008): An invaded wet ecosystem in central Celauro, D. (2006): Pesci: dati preliminari. In: Biodiversità, Italy: an arrangement and evidence for an alien food chain. Gestione e Conservazione di un’Area Umida del Litorale Rendiconti Lincei 19: 161–171. Tirrenico: la Palude di Torre Flavia, p. 234–239. Battisti, C., Ed., Battisti, C., Ed. (2006): Biodiversità, Gestione e Conservazione di Rome, Italy, Gangemi Editore. un’Area Umida del Litorale Tirrenico: la Palude di Torre Flavia. Rome, Italy, Provincia di Roma, Gangemi Editore. Chiesa, S. (2006): Il gambero rosso della Louisiana (Procambarus Bologna, M.A., Capula, M., Carpaneto, G.M. (2000): Anfibi e Rettili clarkii Girard, 1852) nel monumento naturale “Palude di Torre del Lazio. Rome, Italy, Fratelli Palombi Editori. 160 pp. Flavia.” In: Biodiversità, Gestione e Conservazione di un’Area Bologna, M.A., Salvi, D., Pitzalis, M. (2007): Atlante degli Anfibi e Umida del Litorale Tirrenico: la Palude di Torre Flavia, p. 354– Rettili della Provincia di Roma. Rome, Italy, Provincia di Roma, 359. Battisti, C., Ed., Rome, Italy, Gangemi Editore. Assessorato alle politiche agricole e dell’ambiente, Gangemi Da Silva, E., Blasco, M. (1995): Trachemys scripta elegans in First European Records for Kinosternon subrubrum and Pelomedusa olivacea 307

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